Abstract
Background: We determined the predictive accuracy of penile bacteria for incident BV in female sex partners. In this prospective cohort, we enrolled Kenyan men aged 18–35 and their female sex partners aged 16 and older. We assessed BV at baseline, 1, 6, and 12 months. Incident BV was defined as a Nugent score of 7–10 at a follow-up visit, following a Nugent score of 0–6 at baseline. Amplification of the V3–V4 region of the bacterial 16S rRNA gene was performed on meatal and glans/coronal sulcus swab samples. Majority vote classifier combined the decisions of three machine learning classification algorithms (Random Forest, Support Vector Machine, K Nearest Neighbor). We report the estimate cross-validation predictive accuracy for incident BV based on baseline penile taxa.Results: The incidence of BV was 31% among 168 couples in which the woman did not have BV at baseline: 37.3% if the man was uncircumcised vs. 26.3% if the man was circumcised. Incident BV occurred at 1 month (n = 23), 6 months (n = 20), 12 months (n = 9). The predictive capacity of meatal taxa was high: sensitivity (80.7%), specificity (74.6%), accuracy (77.5%), area under the curve (88.8%). Variable importance ranking identified meatal taxa that in the vagina are associated with BV: Parvimonas, Lactobacillus iners, L. crispatus, Dialister, Sneathia sanguinegens, and Gardnerella vaginalis were among the top 10 most predictive taxa. The accuracy of glans/coronal sulcus taxa to predict incident BV was comparable to meatal taxa accuracy, but with greater variability.Conclusions: Baseline penile microbiota accurately predicted BV incidence in women who did not have BV at baseline, with more than half of incident infections observed at 6- to 12- months after penile microbiome assessment. These results suggest interventions to manipulate the penile microbiome may reduce BV incidence in sex partners, and that potential treatment (antibiotic or live biotherapeutic) will need to be effective in reducing or altering bacteria at both the glans/coronal sulcus and urethral sites (as represented by the meatus). The temporal association clarifies that concordance of penile microbiome with the vaginal microbiome of sex partners is not merely reflecting the vaginal microbiome, but can contribute to it.
Highlights
Bacterial vaginosis (BV) is a condition of public health concern, affecting 20–50% of the general population of women in subSaharan Africa (Torrone et al, 2018), and associated with increased risk of HIV acquisition and other sexually transmitted infections (STI) (Atashili et al, 2008; Lewis et al, 2017)
Using assimilation of multiple machine learning classifiers, this study had four main findings: (1) The penile microbiome accurately predicts incident BV in the female sex partner; (2) Prediction accuracy of incident BV in female sex partners was similar for microbiota from the meatus and from glans/coronal sulcus, though results from meatal samples had more stable performance; (3) Several meatal bacteria that were most important in predicting incident BV overlapped with vaginal bacteria commonly associated with BV, which intuitively explains the high predictive accuracy for incident BV in female partners, whereas this was less apparent for bacteria from the glans/coronal sulcus; and (4) Circumcision status had low variable importance in the predictions of incident BV in female partners
One theory is that recovery of penile bacteria that in the vagina are associated with BV, may represent recent or frequent sex and it is the recent or frequent sex that explains the association with BV in the female partner; this explanation cannot account for the differential association between circumcision status and BV observed in our study and others (Gray et al, 2009; Liu et al, 2015)
Summary
Bacterial vaginosis (BV) is a condition of public health concern, affecting 20–50% of the general population of women in subSaharan Africa (Torrone et al, 2018), and associated with increased risk of HIV acquisition and other sexually transmitted infections (STI) (Atashili et al, 2008; Lewis et al, 2017). Female sex partners of Ugandan men undergoing voluntary medical male circumcision (VMMC) had 40% lower prevalence of BV at 1 year (Gray et al, 2009). Mändar et al found a high concordance of microbiota between semen and vaginal samples, supporting their hypothesis that “semen serves as a medium for the transmission of microorganisms between men and women” (Mandar et al, 2015). These studies provide strong evidence for the sexual exchangeability of the vaginal and penile microbiota in relation to BV, and demonstrate that there are multiple male genitourinary reservoirs for these taxa. We report the estimate cross-validation predictive accuracy for incident BV based on baseline penile taxa
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